Toward an Integrative Perspective on Hippocampal Function: From the Rapid Encoding of Experience to Adaptive Behavior

Abstract

The mammalian hippocampus has been associated with learning and memory, as well as with many other behavioral processes. In this article, these different perspectives are brought together, and it is pointed out that integration of diverse functional domains may be a key feature enabling the hippocampus to support not only the encoding and retrieval of certain memory representations, but also their translation into adaptive behavior. The hippocampus appears to combine: (i) sensory afferents and synaptic mechanisms underlying certain types of rapid learning; and (ii) links to motivational, emotional, executive, and sensorimotor functions. Recent experiments are highlighted, indicating that the induction of hippocampal synaptic plasticity is required to encode rapidly aspects of experience, such as places, into memory representations; subsequent retrieval of these representations requires transmission through the previously modified hippocampal synapses, but no further plasticity. In contrast, slow incremental place learning may not absolutely require hippocampal contributions. The neocortical sensory inputs, especially visuo-spatial information, necessary for hippocampus-dependent rapid learning, are preferentially associated with the septal to intermediate hippocampus. In contrast, connectivity with the prefrontal cortex and subcortical sites, which link the hippocampus to motivational, emotional, executive, and sensorimotor functions, is primarily associated with the intermediate to temporal hippocampus. A model of functional differentiation and integration along the septo-temporal axis of the hippocampus is proposed, describing key hippocampal contributions to adaptive behavior based on information encoded during a single or a few past experiences.